Abstract

Background

The F- and V-type ATPases are rotary molecular machines that couple translocation
of protons or sodium ions across the membrane to the synthesis or hydrolysis of ATP.
Both the F-type (found in most bacteria and eukaryotic mitochondria and chloroplasts)
and V-type (found in archaea, some bacteria, and eukaryotic vacuoles) ATPases can
translocate either protons or sodium ions. The prevalent proton-dependent ATPases
are generally viewed as the primary form of the enzyme whereas the sodium-translocating
ATPases of some prokaryotes are usually construed as an exotic adaptation to survival
in extreme environments.

Results

We combine structural and phylogenetic analyses to clarify the evolutionary relation
between the proton- and sodium-translocating ATPases. A comparison of the structures
of the membrane-embedded oligomeric proteolipid rings of sodium-dependent F- and V-ATPases
reveals nearly identical sets of amino acids involved in sodium binding. We show that
the sodium-dependent ATPases are scattered among proton-dependent ATPases in both
the F- and the V-branches of the phylogenetic tree.

Conclusion

Barring convergent emergence of the same set of ligands in several lineages, these
findings indicate that the use of sodium gradient for ATP synthesis is the ancestral
modality of membrane bioenergetics. Thus, a primitive, sodium-impermeable but proton-permeable
cell membrane that harboured a set of sodium-transporting enzymes appears to have
been the evolutionary predecessor of the more structurally demanding proton-tight
membranes. The use of proton as the coupling ion appears to be a later innovation
that emerged on several independent occasions.

Reviewers

This article was reviewed by J. Peter Gogarten, Martijn A. Huynen, and Igor B. Zhulin.
For the full reviews, please go to the Reviewers' comments section.